On September 21, 2002, a pertussis case (confirmed by isolation of Bordetella pertussis) was reported to the Yavapai County
Health Department (YCHD). The patient was a child aged 13 years in the 8th
grade at a middle school in Yavapai County; the child had attended school
during the illness. A case consistent with the clinical definition of pertussis
had been reported in another student in the same classroom 2 weeks earlier.
On September 22, a second culture-confirmed case was reported from the same
classroom. Subsequent investigation identified five additional persons (two
students in the same classroom, two 8th-grade teachers, and one parent of
an ill student) with prolonged cough illnesses. In comparison, during the
previous 10 years, an average of four pertussis cases were reported annually
from this county. On September 26, YCHD, in conjunction with the Arizona Department
of Health Services (ADHS) and school officials, notified the community of
the pertussis outbreak in the middle school and initiated control measures.
This report summarizes the epidemiology of the outbreak and the control measures
used to contain it. Health-care providers should consider pertussis in persons
of any age with acute cough illnesses and consider obtaining nasopharyngeal
(NP) specimens for B. pertussis culture.

A probable case of pertussis was defined as an acute cough illness lasting
≥14 days.1 In a person with ≥1 day
of cough, cases were confirmed by isolation of B. pertussis from an NP specimen. In persons with cough of ≥14 days, cases were
confirmed by either (1) a positive polymerase chain reaction (PCR) test result
for B. pertussis DNA from an NP specimen or (2) epidemiologic
linkage to a person with a laboratory-confirmed case. Epidemiologic linkage
was defined as close contact with a person with laboratory-confirmed pertussis
or attendance at the same school as a person with a laboratory-confirmed case.

Public health and school officials implemented an aggressive control
strategy requiring the exclusion of any coughing student or staff member from
the school through the fifth day of treatment with an antibiotic recommended
for pertussis.1 Parents of excluded students
were given letters advising them to contact their health-care providers for
medical examination, to contact YCHD to have an NP specimen collected for
culture, and to stay at home and away from others (particularly infants and
young children) through the fifth day of treatment. Health-care providers
were alerted to the pertussis outbreak through an existing e-mail and facsimile
network and were urged to send patients with suspected pertussis to YCHD for
NP specimen collection. To attempt isolation of B. pertussis, YCHD forwarded all NP specimens collected to Arizona's Bureau of
State Laboratory Services (BSLS). If identified at another laboratory, B. pertussis isolates were forwarded to BSLS in accordance
with Arizona administrative code. All B. pertussis isolates
were forwarded to CDC for pulsed-field gel electrophoresis (PFGE) profiling.
A sample of NP specimens collected by YCHD was forwarded from BSLS to CDC
for PCR testing. PCR testing targeted genes coding for an insertion element
(IS481) and for pertussis toxin subunit 1 (ptxS1).

On October 24, YCHD and ADHS recommended initiation of an accelerated
pertussis vaccination schedule for infants because of the increasing numbers
of pertussis cases identified throughout six communities in Yavapai County.
On the accelerated schedule, the first 3 doses of the diphtheria and tetanus
toxoids and acellular pertussis (DTaP) vaccine are administered at ages 6,
10, and 14 weeks rather than at the usual recommended ages of 2, 4, and 6
months.2 Other vaccinations recommended
according to the childhood immunization schedule2,3 also
were administered on the accelerated schedule.

A total of 485 pertussis cases were reported from six communities (2000
population: 83,550) in the county (580.5 per 100,000 population): 218 confirmed
cases (16 by isolation of B. pertussis and 202 by
epidemiologic linkage) and 267 probable cases (Figures 1 and 2). Of the 485
cases, 203 (42%) were associated with schools; 113 (56%) were in students,
eight (4%) were in school staff, and 82 (40%) were in family members (including
the nine infants with cases confirmed by epidemiologic linkage) or close contacts
of ill students or staff members. Cases were identified in an elementary school,
a middle school, and a high school (Table). The highest attack rate was among
students in the 8th grade of the middle school; of 198 students in this grade,
20 (10%) were confirmed to have pertussis. Males accounted for 193 (54%) of
357 persons aged ≤19 years and 24 (19%) of 128 persons aged ≥20 years.
The median age of persons with pertussis was 13 years (range: 0-83 years).
Among the 29 infants aged <1 year, 20 (69%) had onset before October 24,
when the accelerated schedule was recommended; of the nine cases that occurred
after October 24, one infant was too young to be vaccinated, seven were aged
≥14 weeks and were ineligible for the accelerated schedule, and one was
eligible but did not receive vaccine according to the accelerated schedule.
DTaP vaccination data were available for 24 (83%) infants: three (13%) infants
were not vaccinated; eight (33%) received 1 DTaP vaccination; five (21%) received
2 DTaP vaccinations; and eight (33%) received 3 DTaP vaccinations. Although
15 (52%) of the 29 infants were aged <6 months, no infants were hospitalized
for pertussis.

Of 1,047 NP samples sent to BSLS, CDC tested 569 (54%) by PCR. Of these
569 samples, 11 (2%) had positive PCR results for B. pertussis DNA, 462 (81%) had negative results, and 96 (17%) could not be tested
because of improper specimen processing or were indeterminate because of contamination.
Of the 11 persons with positive PCR results, 10 (91%) also had B. pertussis isolated at BSLS. The one case with a positive PCR result
and a negative culture result was in a person in close contact with a person
from whom B. pertussis was isolated.

All 16 B. pertussis isolates were profiled
genetically by PFGE, and four profiles were identified: profile 10 (63%),
profile 160 (25%), profile 13 (6%), and profile 55 (6%). Profile 10 was identified
in B. pertussis isolates from epidemiologically linked
patients attending the middle and high school. Seven of the eight isolates
from middle school students were profile 10; these seven students were linked
epidemiologically and had cough onset within 1 month of each other. The eighth
student had onset of pertussis 3 months later, and the isolate was PFGE profile
55.

The outbreak peaked in mid-October and lasted 6 months. The last culture-positive
case occurred in a person who had cough onset on January 10, 2003.

Middle and high school–associated pertussis outbreaks are recognized
increasingly and reported to state health departments, but few outbreak investigation
results are published.1,4 The
Yavapai outbreak shared features of many of these outbreaks, including a substantial
number of cases among older children and adolescents (i.e., persons aged 10-19
years) and subsequent spread to the community, with cases among infants aged
<1 year. In the United States, cases in older children and adolescents
are reported most commonly in the fall, when students return to school.5 Because of waning immunity, older children and
adolescents can become susceptible to pertussis 5-15 years after the last
DTaP dose.6 In 2002, pertussis cases in
persons aged 10-19 years constituted 29% (7.0 per 100,000 population) of 9,771
nationally reported cases (CDC, unpublished data, 2003). In the six affected
communities in Yavapai County, the incidence of confirmed and probable pertussis
among older children and adolescents was 1,348 per 100,000 population.

Attack rates among children in the three schools differed by school
and grade. The outbreak was recognized first among students in the 8th grade
of the middle school, which had higher attack rates than either the elementary
or the high school. Although control measures implemented when the outbreak
was identified appear to have contributed to lower attack rates in the elementary
and high schools, differences in susceptibility, efficiency of transmission,
or mixing patterns also might have been factors. The coverage level for ≥4
DTaP doses among children entering elementary school was >90% (ADHS, unpublished
data, 2003); these children probably had immunity from recent DTaP vaccination.
Although high school students can be susceptible to pertussis, and high attack
rates have been documented,1,4 immunity
boosted by exposure to B. pertussis before this outbreak
might account for the low attack rate at this school.

In this outbreak, CDC's PCR testing was as specific as B. pertussis isolation but not more sensitive in confirming B. pertussis infection. The concordance of results was high and probably
reflects the use of two sets of primers and a stringent quality-assurance
program that detected false-positive results. In other pertussis outbreaks
in which different PCR primers and protocols were used, cases with PCR-positive
but culture-negative results were identified. Although they are widely used
in the United States, PCR assays have not been standardized, and their predictive
value for pertussis is unknown. Exclusive use of nonstandardized PCR assays
can result in either underestimation or overestimation of pertussis.1,7

As in other school outbreaks,8 a single
PFGE profile predominated among the middle school isolates, indicating student-to-student
spread. Communitywide outbreaks have been associated with an increase in B. pertussis infections with PFGE profiles that predominated
before the epidemic.9 Although minimal data
are available on the profiles of strains circulating in Yavapai County before
the outbreak, outbreak PFGE profiles 10 and 13 were identified among 165 sporadic
isolates recovered in Arizona during 1999-2003 (CDC, unpublished data, 2003).

The data described in this report are subject to at least two limitations.
First, because persons can have cough of ≥14 days from other illnesses,
the use of the probable case definition and epidemiologic linkage to confirm
cases in Yavapai County might have led to an overestimation of the size of
the outbreak. However, although pertussis is challenging to confirm, studies
of pertussis incidence have documented that passive reporting underestimates
pertussis incidence.1,5,6 The
absence of severe illness among infants could have resulted from the lack
of specificity of the case definition used; milder illness also is consistent
with DTaP vaccine–induced protection. Second, because the epidemic peak
coincided with the time that the accelerated DTaP vaccination schedule was
recommended, the impact of this recommendation could not be evaluated. Additional
studies are needed to evaluate the effectiveness of the accelerated schedule.

Although infants with pertussis can become severely ill and die,5,10 no pertussis-associated hospitalizations
or deaths were reported during this outbreak. In contrast to disease severity
observed commonly among infants, older persons with pertussis often have a
mild illness. As a result, older persons might not visit a health-care provider
until several weeks after cough onset, when recovery of the fastidious B. pertussis bacterium is unlikely and diagnosis might
not be confirmed.6 Recognizing pertussis
outbreaks in schools is challenging for several reasons, including (1) patients
usually do not seek medical care early, (2) a diagnosis of pertussis might
be delayed or not considered, and (3) the sensitivity and specificity of diagnostic
tests will be low if NP specimens are not obtained and transported to the
laboratory under optimal conditions. Health-care providers should consider
pertussis in persons of any age with an acute cough illness and consider obtaining
NP specimens for B. pertussis culture. Early recognition,
treatment, and chemoprophylaxis can help prevent transmission to others; because
of its severity in young unvaccinated infants, preventing pertussis in this
population is of greatest importance.1,4,5,10